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Smoking and the sudden infant death syndrome: results from 1993-5 case-control study for confidential inquiry into stillbirths and deaths in infancy

^a Foundation for the Study of Infant Deaths Research Unit, Institute of Child Health, Royal Hospital for Sick Children, Bristol BS2 8BJ, ^b Operational Research Division, NHS Executive, Quarry House, Leeds LS2 9UA, ^c Nuffield Institute for Health, Leeds LS2 9PL, ^d Friarage Hospital, Northallerton, North Yorkshire DL6 1JG, ^e Sheffield Children's Hospital, Sheffield S10 2TH, ^f University of Bristol, St Michael's Hospital, Bristol BS2 8EG, ^g Institute of Child Health, Royal Hospital for Sick Children, Bristol BS2 8BJ, ^h Department of Child Health, Postgraduate Medical School, Royal Devon and Exeter Hospital, Exeter EX2 5DW

The regional coordinators and researchers of the confidential inquiry into stillbirths and deaths in infancy are given at the end of this article. Correspondence to: Professor Fleming.

Abstract

Objective: To investigate the effects of exposure to tobacco smoke and of parental consumption of alcohol and illegal drugs as risk factors for the sudden infant death syndrome after a national risk reduction campaign which included advice on prenatal and postnatal avoidance of tobacco smoke.
Design: Two year population based case-control study. Parental interviews were conducted for each infant who died and four controls matched for age and date of interview.
Setting: Three regions in England with a total population of 17 million people.
Subjects: 195 babies who died and 780 matched controls.
Results: More index than control mothers (62.6% v 25.1%) smoked during pregnancy (multivariate odds ratio = 2.10; 95% confidence interval 1.24 to 3.54). Paternal smoking had an additional independent effect when other factors were controlled for (2.50; 1.48 to 4.22). The risk of death rose with increasing postnatal exposure to tobacco smoke, which had an additive effect among those also exposed to maternal smoking during pregnancy (2.93; 1.56 to 5.48). The population attributable risk was over 61%, which implies that the numbers of deaths from the syndrome could be reduced by almost two third if parents did not smoke. Alcohol use was higher among index than control mothers but was strongly correlated with smoking and on multivariate analysis was not found to have any additional independent effect. Illegal drug use was more common among the index parents, and paternal use of illegal drugs remained significant in the multivariate model (4.68; 1.56 to 14.05).
Conclusions: This study confirms the increased risk of the sudden infant death syndrome associated with maternal smoking during pregnancy and shows evidence that household exposure to tobacco smoke has an independent additive effect. Parental drug misuse has an additional small but significant effect.

Introduction

Although the incidence of sudden unexpected deaths in infancy in the United Kingdom has fallen, especially since the "Back to Sleep" campaign in 1991, such deaths remain the largest single group of deaths of infants between 1 week and 1 year old.¹ The study of sudden unexpected deaths in infancy (part of the national confidential inquiry into stillbirths and deaths in infancy (CESDI), funded by the Department of Health) conducted a detailed case-control study and confidential inquiry of all sudden unexpected deaths in infancy in the participating regions of the United Kingdom in the two year period one year after the national intervention campaign. A summary of the preliminary results of this study has been published.²

Several case-control studies have shown an association between the risk of maternal smoking during pregnancy and the sudden infant death syndrome.^{3 4 5 6 7 8 9 10 11 12 13} A recent meta-analysis of these studies, including cohort and smaller case-control studies, estimate a pooled relative risk (adjusted for prone sleeping position) of 2.99 (95% confidence interval 2.79 to 3.19) for maternal smoking during pregnancy.¹² Many of these studies, however, were conducted before the recent decreases in the incidence of such deaths which followed risk reduction campaigns in several countries.

Several studies have shown evidence of increasing risk of the syndrome with increasing exposure to tobacco smoke within the household.^{6 13 14 15} We investigated the risk of the sudden infant death syndrome associated with exposure to tobacco smoke after the national campaign to reduce the risk of such deaths. Exposure was measured in terms of both the in utero effect and the effect once the infant is born. The effects of alcohol consumption and parental use of illegal drugs in relation to smoking were also studied.

Methods

STUDY DESIGN, CASE NOTIFICATION, AND SELECTION OF CONTROLS

The study aimed to include all cases of the sudden infant death syndrome in infants aged 7 to 364 days inclusive in two NHS regions in the United Kingdom (Southwest and Yorkshire) from February 1993 and a third region (Trent) from September 1993 until January 1995 inclusive, the total population of the study area being about 17 million.

As in previous studies in Avon, Sheffield, and Yorkshire cases were ascertained by means of a communication network of professionals and lay organisations who reported all deaths within 24 hours. All sudden unexpected deaths in infancy were initially reported and investigated.

Data were collected on a standard questionnaire by four research interviewers for each region, consistency of approach being maintained by cross regional initial training and regular meetings thereafter. Four controls for each case were selected by the method previously used in Avon.^{16 17 18} The same interviewer visited each control family, usually within a week of the death, to collect the same data as for the index case.

Full details of the methods and the statistical analysis are given in the accompanying paper.¹⁹

Results

Ascertainment of cases and controls--Details of the ascertainment are given in the accompanying paper.¹⁹ During the study period, 266 sudden unexpected deaths in infancy were identified, of which 216 were classified as the sudden infant death syndrome. This analysis deals with the 195 babies who died (90.3% of the total) for whom full data are available and their 780 matched controls.

Time to first interview--The median time from the discovery of the death until the first interview of the index parents was 4.5 days; 82% of families were interviewed within 14 days and 95% within 28 days of the death.

Matching for age--Over two thirds of the controls were matched within 2 weeks and over 90% within 1 month of the age of the index baby.

SMOKING

Table 1 shows the univariate statistics (controlled for matching) for maternal smoking before, during, and after pregnancy; paternal smoking; and others, excluding parents, who smoked in the household.

Table 1--Univariate statistics for smoking and sudden infant death syndrome
---------------------------------------------------------------------------
                                                        Odds ratio
                           No (%) of     No (%) of   (95% confidence
Detail                  babies who died   controls      interval)
---------------------------------------------------------------------------
Maternal smoking:
 Before pregnancy       138 (70.8)       255 (32.7)  5.07 (3.45 to 7.45)
 During pregnancy       122 (62.6)       196 (25.1)  4.84 (3.33 to 7.04)
 After pregnancy        129 (66.2)       209 (26.8)  5.19 (3.57 to 7.55)
Paternal smoking        118 (60.5)       282 (36.2)  3.04 (2.13 to 4.36)
Others smoking in home   28 (14.3)        46 (5.9)   2.99 (1.71 to 5.25)

The majority of both index and control mothers (85.7% and 87.5%, respectively) remained smokers or non-smokers in the periods before, during, and after pregnancy. Table 2 shows the dose-response effects of exposure to tobacco smoke. The more the mother smoked during pregnancy the greater the associated risk. For other household members this trend was less clear.

Table 2--Dose-response effects of smoking on risk of sudden infant death syndrome
--------------------------------------------------------------------------------------
                                                             Odds ratio
                                No (%) of     No (%) of   (95% confidence
No of cigarettes smoked      babies who died  controls        interval)
--------------------------------------------------------------------------------------
Mother during pregnancy:
 None                        73 (37.4)        584 (74.9)          1.00
 1-9                         53 (27.2)        108 (13.8)  4.59 (2.71 to 7.77)
 10-19                       42 (21.5)         58 (7.4)   5.38 (2.96 to 9.75)
 >/=20                       27 (13.8)         30 (3.8)   7.88 (3.87 to 12.26)
Father:
 None                        77 (39.5)        498 (63.8)          1.00
 1-9                         33 (16.9)        100 (12.8)  2.18 (1.28 to 3.69)
 10-19                       52 (26.7)        112 (14.4)  3.81 (2.31 to 6.29)
 >/=20                       33 (16.9)         70 (9.0)   3.50 (1.86 to 6.56)
Others (excluding parents):
 None                        167 (85.6)       734 (94.1)          1.00
 1-9                           6 (3.1)         15 (1.9)       P = 0.257*
 10-19                         7 (3.6)         15 (1.9)       P = 0.161*
 >/=20                        15 (7.7)         16 (2.1)   4.12 (1.85 to 9.08)
--------------------------------------------------------------------------------------
*Fisher's exact test; if these groups are combined: odds ratio = 1.96 (0.93 to 4.13).

Table 3 shows that smoking by partners and others in the household was both significant and independent of maternal smoking during pregnancy. The data suggest that the risks associated with tobacco smoke are not restricted to an in utero effect from maternal smoking. Table 4 shows the effect of postnatal exposure to tobacco smoke. The first two measures show the number of smokers and the number of cigarettes smoked daily in those households where smoking was allowed in a room with the baby present. The third measure gives a parental estimation of the infants' daily exposure to smoke, both within and outside the household. The risk increased with increasing numbers of smokers in the household, increasing total number of cigarettes smoked a day, and increasing daily exposure to tobacco smoke.

Table 3--Effects of smoking by fathers and others (excluding parents) in households,
controlled for maternal smoking during pregnancy on risk of sudden death syndrome
---------------------------------------------------------------------------------------
                                                                     Odds ratio
                                        No (%) of     No (%) of   (95% confidence
Smoking status                       babies who died  controls       interval)
---------------------------------------------------------------------------------------
Father non-smoker/mother non-smoker   33 (16.9)       421 (54.0)          1.00
Father smoker/mother non-smoker       40 (20.5)       163 (20.9)  3.41 (1.98 to 5.88)
Father non-smoker/mother smoker       44 (22.6)        77 (9.9)   7.01 (3.91 to 12.56)
Father smoker/mother smoker           78 (40.0)       119 (15.3)  8.41 (5.08 to 13.92)
Other non-smoker/mother non-smoker    65 (33.3)       561 (71.9)          1.00
Other smoker/mother non-smoker         8 (4.1)         23 (2.9)        P = 0.007*
Other non-smoker/mother smoker       102 (52.3)       173 (22.2)  6.01 (4.12 to 8.78)
Other smoker/mother smoker            20 (10.3)        23 (2.9)   7.27 (3.46 to 14.94)
---------------------------------------------------------------------------------------
*Fisher's exact test.

Table 4--Postnatal exposure to tobacco smoke and risk of sudden death syndrome
--------------------------------------------------------------------------------------------------------------
                                                                                   Odds ratio
                                                      No (%) of     No (%) of   (95% confidence
Level of exposure                                  babies who died  controls        interval)
--------------------------------------------------------------------------------------------------------------
No of smokers in household*:
 None                                              101 (52.3)       615 (80.4)           1
 1                                                  22 (11.4)        66 (8.6)    2.44 (1.36 to 4.37)
 2                                                  59 (30.6)        77 (10.1)   5.15 (3.24 to 8.21)
 >/=3                                               11 (5.7)          7 (0.9)   10.43 (3.34 to 32.54)
 No with data available                              193              765
No of cigarettes smoked daily*:
 None                                              101 (52.3)       615 (80.4)            1
 1-19                                               18 (9.3)         56 (7.3)    2.47 (1.29 to 4.73)
 20-39                                              40 (20.7)        67 (8.8)    3.96 (2.40 to 6.55)
 >/=40                                              34 (17.6)        27 (3.5)    7.57 (4.00 to 14.32)
 No with data available                              193              765
Infant's daily exposure to tobacco smoke (hours):
 0                                                  85 (45.7)       593 (76.9)            1
 1-2                                                26 (14)          90 (11.7)   1.99 (1.14 to 3.46)
 3-5                                                22 (11.8)        45 (5.8)    3.84 (1.97 to 7.48)
 6-8                                                19 (10.2)        18 (2.3)    6.78 (3.17 to 14.49)
 >8                                                 34 (18.3)        25 (3.2)    8.29 (4.28 to 16.05]
 No with data available                              186+             771+
--------------------------------------------------------------------------------------------------------------
*In households where smoking was allowed in the same room as the infant.
+Of the nine sets of index and control parents who did not answer this question, at least one parent smoked.

SMOKING AND ALCOHOL CONSUMPTION

There was no significant difference between the index and control partners regarding usual alcohol consumption (P = 0.901) or consumption of 3 or more units (17.3% v 15.2%) within 24 hours of the final or reference sleep (odds ratio = 1.24; 95% confidence interval 0.80 to 1.90). Table 5 shows the weekly alcohol consumption of index and control mothers before pregnancy and consumption within the last 24 hours. The linear comparison of usual consumption was not significant (P = 0.053). The index mothers tended either to drink no alcohol or to drink more than 10 units a week. For those drinking more than 10 units a week most index and control mothers decreased their alcohol consumption during pregnancy (73.9% v 85.4%), but significantly fewer index mothers (39.1% v 77.1%) decreased their consumption after pregnancy (5.23; 1.58 to 17.61).

Table 5--Maternal alcohol consumption and risk of sudden death syndrome
--------------------------------------------------------------------------------------------
                           No (%)                  Odds ratio (95% confidence interval)
Consumption of alcohol    of babies     No (%)     -----------------------------------------
(units)                  who died    of controls  Not adjusted          Adjusted*
--------------------------------------------------------------------------------------------
Weekly before pregnancy:
 1-10                      75 (39.7)  396 (50.9)          1.00+                1.00+
 None                      91 (48.1)  333 (42.9)   1.44 (1.01 to 2.06)  1.34 (0.90 to 1.99)
 >10                       23 (12.2)   48 (6.2)    2.68 (1.46 to 4.82)  1.82 (0.96 to 3.46)
In past 24 hours:
 0-2                      168 (88.5)  743 (95.5)          1.00+                1.00+
 >/=3                      22 (11.5)   35 (4.5)    2.62 (1.40 to 4.90)  1.91 (0.97 to 3.76)
--------------------------------------------------------------------------------------------
*Adjusted for maternal smoking.
+Reference group.

Usual alcohol consumption became non-significant when we adjusted for socioeconomic status (no alcohol: 1.22; 0.81 to 1.85; >10 units a week: 1.75; 0.91 to 3.36). Alcohol consumption in the last 24 hours became non-significant when we further adjusted for maternal smoking (1.62; 0.53 to 4.91).

SMOKING AND ILLEGAL SUBSTANCE USE

The parents were given a list of illegal drugs and asked if they had taken any of these more than once. The list included heroin, crack, cocaine, ecstasy, speed, LSD, amphetamines, barbiturates, cannabis, and glue. We expected that parents might be reluctant to answer this question, but in the event they did so readily. Table 6 shows the results.

Table 6--Parental use of illegal drugs and risk of sudden infant death syndrome
-------------------------------------------------------------------------------------------------
                        No (%)                     Odds ratio (95% confidence interval)
                    of babies who    No (%)        ----------------------------------------------
Drug use                 died      of controls     Not adjusted             Adjusted*
-------------------------------------------------------------------------------------------------
Mother:
 Before pregnancy   31/191 (16.2)  41/778 (5.3)  3.93 (2.18 to 7.09)   2.37 (1.25 to 4.47)
 During pregnancy   16/190 (8.4)   11/775 (1.4)  7.05 (2.58 to 19.29)  4.34 (1.51 to 12.43)
 After pregnancy    16/191 (8.4)   19/777 (2.4)  4.54 (1.92 to 10.71)  2.80 (1.10 to 7.18)
Partner:
 Year before birth  37/172 (21.5)  50/755 (6.6)  3.76 (2.21 to 6.37)   3.28 (1.88 to 5.71)
 After birth        29/169 (17.2)  31/753 (4.1)  5.35 (2.71 to 10.53)  4.18 (2.06 to 8.48)
------------------------------------------------------------------------------------------------
*Adjusted for maternal (before, during, or after pregnancy) and paternal smoking as appropriate.

By far the commonest drug used was cannabis, which was used by 6.8% of index mothers during pregnancy and 1% of control mothers. The use of illegal drugs among parents remained a significant risk factor even after adjustment for tobacco smoking.

MULTIVARIATE ANALYSIS

Several factors remained significant in the multivariate analysis but are not amenable to change. These included younger mothers, mothers without a partner, high parity, multiple births, short gestation, and low socioeconomic status. After we controlled for all of these factors along with sleeping position and possible confounders such as maternal alcohol consumption, parental use of illegal drugs, parental bed sharing, and the protective effect of breast feeding maternal smoking during pregnancy remained significant (2.10; 1.24 to 3.54). When we added birth weight (adjusted for gestation and sex) to the model as a known outcome, maternal smoking during pregnancy remained significant (1.78; 1.04 to 3.05). Paternal smoking had an additional independent effect (2.50; 1.48 to 4.22), but smoking by other members of the household became non-significant. The risk associated with smoking if one or both parents smoked was 3.79 (2.09 to 6.88) when we controlled for other factors. In only 16.9% of index households did neither parent smoke; the population attributable risk for smoking by at least one parent was 61.2%.²⁰ When we considered parental estimation of the infant's daily exposure to tobacco smoke as a postnatal marker for smoking, this marker was significant when we controlled for other factors (P = 0.008). If maternal smoking during pregnancy was added to the model, however, the postnatal marker lost its independent effect (P = 0.1601). This may be explained by the strong correlation between maternal smoking during and after pregnancy. The additive effect of smoking in pregnancy and postnatal exposure was significant (2.93; 1.56 to 5.48).

Maternal use of illegal drugs became non-significant in the multivariate model, whether we looked at use before, during, or after pregnancy. Paternal use of illegal drugs after the baby's birth remained significant in the multivariate model (4.68; 1.56 to 14.05).

Discussion

The results of this study, the first after the national intervention campaign, give the strongest evidence to date of the risk of the sudden infant death syndrome associated with smoking. Even after we had controlled for a wide range of confounders, including socioeconomic status, maternal smoking during pregnancy remained significant. Furthermore, we were able to show a biological gradient: the more the mother smoked the greater the risk to the infant. Paternal smoking had an additional independent effect when we controlled for other factors including maternal smoking during pregnancy. In 83.1% of index households at least one parent smoked. The population attributable risk of 61.2% implies that the number of deaths from the syndrome could be reduced by almost two thirds if parents did not smoke. The risk to the infant is therefore twofold: from maternal smoking during pregnancy and from those that smoke either in the presence of the pregnant mother or in the presence of the infant. Trying to quantify the risk of the separate effects is difficult because many of the mothers who smoke during pregnancy are a main source of exposure after pregnancy. Evidence that postnatal exposure has a dose related effect is very strong, however, whether measured by the number of smokers in the household, the number of cigarettes the infant is exposed to, or the number of hours of exposure. Those infants exposed both to maternal smoking during pregnancy and postnatal tobacco smoke are at increased risk.

The index mothers drank slightly more alcohol, but these differences were not significant when we adjusted for maternal smoking. A worrying finding from this study is the use of illegal drugs by the parents. Although the numbers are small and partly reflect the social deprivation of the index group, drug use among the index partners after pregnancy remained a significant risk after many other factors were controlled for.

CONCLUSION

Despite clear health warnings, many people continue to smoke. The responsibility of minimising the risk of the sudden infant death syndrome lies not just with the mother who smokes but all smokers. An appropriate public health message might be that smoking in the same environment as a pregnant mother or child is as unacceptable as drinking and driving. Parents who have been unable to give up or reduce their smoking habit should be strongly advised to keep their baby in a "smoke-free zone." This, however, should not be regarded as an alternative to the much better precaution of not smoking at all.

The regional coordinators of the confidential inquiry into stillbirths and deaths in infancy were Ms Lesley Anson (Yorkshire); Mrs Rosanne Sodzi (South Western, 1993-5); Mrs Rosie Thompson (South Western, from 1995); Ms Sue Wood (Trent). The research health visitors of the inquiry were Mrs Christine Ahronson, Mrs Lindsay Cansfield, Mrs Carmel Davis, Mrs Margaret Griffin, Mrs Pat Johnson, Mrs Lynette Lovelock, Mrs Lynne Middleton, Mrs Pam Mueller, Mrs Shirley Stephenson, Mrs Dawn Taylor, Mrs Lorraine Wright, and the research midwives were Mrs Chris Laws and Mrs Rosie McCabe.

Funding: National Advisory Body for the confidential inquiry into stillbirths and deaths in infancy.

Conflict of interest: None.

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